Spatially explicit phylogeographical reconstruction sheds light on the history of the forest cover in the Congo Basin

Abstract

Aim The impact of Pleistocene climatic oscillations on the biodiversity of African tropical rain forests remains poorly understood, and the Congo Basin is particularly understudied. We aim to elucidate how Pleistocene climatic oscillations shaped lowland tropical rain forests by investigating the intraspecific diversity and evolutionary history of a widespread tree species. Location Guineo‐Congolian rain forest, Central Africa. Taxon Staudtia kamerunensis Warb. (Myristicaceae). Methods We used genome skimming combined with maximum likelihood and Bayesian inference to infer the plastid phylogeny. We estimated the time of speciation and differentiation, genetic diversity, and we employed a continuous phylogeographical approach to infer the dispersal history of its plastid lineages. Results We sequenced an average of 5,827,783 reads per sample, and the reconstructed reference plastome had a mean depth of 73.3. We identified five plastid lineages that diverged during the Early or Middle Pleistocene and are parapatric, suggesting past population fragmentation. Four lineages are endemic to Lower Guinea, and one spans the Congo Basin. We found contrasting patterns of expansion in the two regions, with a rapid and recent range expansion of the Congolian lineage in the last 200,000 years, while the spread of the Lower Guinean lineages was substantially slower. Main conclusion The contrasting demographic histories between eastern and western lineages, associated with contrasted levels of plant species richness and rates of endemism, suggest that forest cover was more stable in Lower Guinea during the Late Pleistocene than in Congolia, where the biodiversity might have been eroded before the forest re‐expanded in the Congo basin. This study illustrates how a continuous phylogeographical inference approach, mostly applied so far for inferring the spread of fast‐evolving pathogens over months or years, can provide new insights to reconstruct the dispersal history of tropical tree species over thousands or millions of years.

Genetic breaks caused by ancient forest fragmentation: phylogeography of Staudtia kamerunensis (Myristicaceae) reveals distinct clusters in the Congo Basin

“…However, "LG North" and "LG South" individuals in this area cannot be distinguished based on their psbA-trnH chloroplast haplotype (dispersed through seeds), which is shared with other "LG South" individuals that occur more southward. The fact that this east-west break in Gabon observed from chloroplast sequence data (also confirmed with S. kamerunensis plastome data; Matvijev et al 2022) is partly erased at the level of the nuclear DNA indicates that gene flow through pollen is more extensive than through seeds. This discordance in nuclear-chloroplast genomic divergence is also observed in the Mayumbe region (i.e., different plastid lineages in southern Congo vs. southwestern DR Congo, but the same nuclear cluster assignment) and around the Cameroon Volcanic Line (i.e., different plastid lineages north and south of the CVL, but the same nuclear cluster assignment; Matvijev et al 2022).…”

“…However, the proportion of individuals with mixed "Congo North" and "Congo South" ancestry is relatively high in the transition zone between the different vegetation types, which indicates that gene flow between both clusters is frequent in their contact zone. Interestingly, the genetic break in south-eastern DR Congo we identified using nuclear SSR data is not observed in phylogeographic analyses using plastome data (Matvijev et al 2022), since plastid lineages in southern and eastern DR Congo are genetically similar to those in northeast DR Congo. This disparity in plastid and nuclear lineage distribution could be caused by selection on the nuclear genome if the "Congo South" cluster developed new adaptations to its peculiar habitat.…”

“…Interestingly, while admixture between the different genetic clusters is abundant in Gabon, no individuals with mixed "LG North" and "LG-Congo" ancestry are observed in Cameroon, although both clusters are geographically close. This is likely because secondary contact between both clusters in Cameroon is relatively recent, which is supported by phylogeographic analyses that reconstructed the dispersal history of S. kamerunensis plastomes (Matvijev et al 2022). This phylogeographic reconstruction shows that the populations in southeast Cameroon are the result of Congolian populations that expanded into northern Congo and southern CAR, and subsequently into Cameroon.…”

“…This disparity in plastid and nuclear lineage distribution could be caused by selection on the nuclear genome if the "Congo South" cluster developed new adaptations to its peculiar habitat. Additionally, the genetic break observed between plastid lineages in central DR Congo (Matvijev et al 2022) is erased at the nuclear DNA, but the break between clusters in western DR Congo might be maintained because of a limited gene flow between populations in swamp forests ("LG-Congo") and semi-deciduous forests ("Congo North").…”

“…A phylogeographic study of the plastomes of S. kamerunensis revealed five main genetic lineages occurring in parapatry, four of them in Lower Guinea and one in Congolia (Matvijev et al 2022). The Congolian lineage had a more recent origin and showed traces of relatively recent range expansion (in the last 200,000 years), generating three parapatric sub-lineages, while the Lower Guinean lineages did not show traces of recent range expansion.…”